Elsevier

Bioresource Technology

Volume 102, Issue 1, January 2011, Pages 324-333
Bioresource Technology

Review
Cathodes as electron donors for microbial metabolism: Which extracellular electron transfer mechanisms are involved?

https://doi.org/10.1016/j.biortech.2010.07.008Get rights and content

Abstract

This review illuminates extracellular electron transfer mechanisms that may be involved in microbial bioelectrochemical systems with biocathodes. Microbially-catalyzed cathodes are evolving for new bioprocessing applications for waste(water) treatment, carbon dioxide fixation, chemical product formation, or bioremediation. Extracellular electron transfer processes in biological anodes, were the electrode serves as electron acceptor, have been widely studied. However, for biological cathodes the question remains: what are the biochemical mechanisms for the extracellular electron transfer from a cathode (electron donor) to a microorganism? This question was approached by not only analysing the literature on biocathodes, but also by investigating known extracellular microbial oxidation reactions in environmental processes. Here, it is predicted that in direct electron transfer reactions, c-type cytochromes often together with hydrogenases play a critical role and that, in mediated electron transfer reactions, natural redox mediators, such as PQQ, will be involved in the bioelectrochemical reaction. These mechanisms are very similar to processes at the bioanode, but the components operate at different redox potentials. The biocatalyzed cathode reactions, thereby, are not necessarily energy conserving for the microorganism.

Introduction

Bioelectrochemical systems (BESs) have become an exciting bioprocessing technology in the field of environmental engineering because of the promise of waste(water) treatment with sustainable bacterial metabolic reactions that use the anode as an electron acceptor. While originally mainly anodic biocatalytic reactions were targeted (with abiotic cathodic reactions), recent interest in biologically-catalyzed cathodic reactions opens new sustainable bioprocessing possibilities, such as: (1) sustainable treatment of waste(water); (2) carbon dioxide offsets; (3) production of chemicals; and (4) clean up of recalcitrant chemicals (bioremediation). In this review, the possible extracellular electron transfer (EET) mechanisms for the microbial electron uptake from a cathode are reviewed, but first a short classification of the underlying principles of microbial BESs are given: coupling electron-donating reactions to electron-accepting reactions.

Initially, workers used the spontaneous electron movement between electronegative bioanodes and electro positive abiotic cathodes in microbial fuel cells (MFCs) to generate electric power (Logan et al., 2006). However, unsustainable and/or expensive cathode systems were used, such as coatings of the noble metal platinum (Pt) to catalyze the oxygen reduction reaction or ferricyanide as a terminal electron acceptor, which is detrimental to further scale up in waste(water) treatment scenarios. To circumvent this problem, Clauwaert et al., 2007a, Clauwaert et al., 2007b operated MFCs with biocathodes at which bacteria catalyze the electron transfer from the cathode to electro positive terminal electron acceptors, such as oxygen or nitrate. This resulted in a complete biological MFC with both bacteria at the anode and cathode, and therefore self-replenishing biological catalysts on just electrode materials, such as carbon or graphite (further examples are given in Table 1). Besides the circumvention of expensive metal catalysts, exciting recent work has shown that biocathodes in photosynthetic MFCs can also reduce carbon dioxide (CO2) (Cao et al., 2009). In regards to the economical viability of BES technology, carbon recycling may become very important, especially for a political climate in which lowering the carbon footprint will have a monetary value.

Preliminary calculations have shown that the economic value of the generated electric power by MFCs from wastewater treatment is currently insufficient to warrant a large investment into BES technology, but that offsetting conventional costs of treatment with activated sludge would aid in returning the investment (Fornero et al., 2010). A recently published life-cycle assessment showed that producing a chemical product, such as hydrogen (or in their case hydrogen peroxide), at the cathode would provide considerably larger environmental benefits compared to generating electric power with MFCs (Foley et al., 2010). In addition, such product would also generate a larger monetary pay back that is necessary to warrant the investment, especially when the chemical product is useful at the wastewater treatment plant (Rosenbaum et al., 2010a). However, to generate a product, such as hydrogen, at the cathode, thermodynamic constraints must be overcome by providing an artificial potential increase between the anode and cathode (Logan et al., 2008, Rozendal et al., 2006). This is mostly performed with a 2-electrode BES for which the worker sets the potential difference between the electrodes by using a potentiostat or power supply, and this is referred to as a microbial electrolysis cell (MEC). MECs obtain all electrons to maintain a half reaction at the cathode from the anodic oxidation of organic material in waste(water). Therefore, the power supply is not the source of electrons, but rather it just overcomes cathodic reaction overpotentials by increasing the potential difference between the two electrodes. In other words, without the external power supply the desired reaction on the cathode cannot occur. Biocathodes in MECs have been used, for example, by Rozendal et al. (2008) to produce hydrogen and by Cheng et al. (2009) to produce methane from CO2 (Table 1).

Several researchers have shown that an optimum anode potential should be maintained to guarantee efficient BES performance and anodic wastewater treatment (Aelterman et al., 2008, Torres et al., 2009, Wei et al., 2010). This can be performed with a 3-electrode BES for which the worker sets the working electrode potential (in this case for optimum anodic potentials) by using a potentiostat and a reference electrode, such as a Ag/AgCl reference system. Here, this BES is referred to as a microbial 3-electrode cell (M3C). Vice versa, the set potential at the working electrode can also maintain optimum cathodic potentials to, for example, support a bioelectrochemical electron-accepting reaction. Thus, an M3C can be regarded as a special case of an MEC for which an external power input helps to drive the reaction, while one electrode potential (working electrode) is controlled at favorable electrochemical conditions. Even more importantly, through optimization of the reaction rate, the M3C can boost the current density, which is also pertinent to ensure an economical scale up. Foley et al. (2010) have suggested a requirement of 1000 A/m3 for a successful pilot or full-scale project, and such a high current is feasible with an M3C because after setting the working electrode potential (vs. the reference electrode), the maximum bioelectrochemical reaction rates at the working electrode are achieved by an automated increase in the potential difference between anode and cathode (the worker does not set the potential difference). Although this may require potentials ∼2 V, this can still be economical if a product is formed with an added value that is higher than the value of electric energy consumed by the power supply. However, scale up of M3Cs may be difficult due to problems with maintaining a set working electrode potential for large surface areas. M3Cs without membranes (potentiostat-poised half cells) have been used to proof the concept of biocathodes even before applications in MFCs were considered (He and Angenent, 2006). Recently, M3Cs have been used to sustain biocathodes as powerful new devices for bioremediation applications, such as the reduction of chlorinated compounds (Aulenta et al., 2010), uranium (Gregory and Lovley, 2005), or chromium [(Tandukar et al., 2009) – here operated as an MFC, but M3C application is feasible] (more examples are given in Table 1).

Section snippets

Biocathodic electron transfer mechanisms

Although an increasing number of biocathode studies were published in recent years (e.g., 2 publications in 2004; 12 in 2007; and 34 in 2009; Source: Web of Knowledge, keyword “biocathode∗”, April 26, 2010) (Table 1), not much is known about the biochemical mechanisms of microbial electron uptake from a cathode. The main goal for this review is to suggest and discuss an array of possible bioelectrochemical electron-accepting reaction – none of which has been fully experimentally proven. This

Outlook

With increasing interest in the application of electrodes as electron donors for a large number of microbially-catalyzed reactions of industrial or environmental relevance, the biochemical mechanisms involved in microbial electron uptake from a cathode are required to be uncovered. In this review, possible strategies that microorganisms can employ to exploit electrodes as electron donors for their metabolisms were elucidated and proposed. It is now the task of the scientific community to

Conclusions

A deep understanding of the biochemical energetics of the reaction mechanisms to optimize functional biocathodes is necessary. This is important because the energy gain for biocathode application must be maximized, and therefore the energy consumption by the microorganism should be minimized. It was discussed, here, that the microbial energy gain of biocathodic reactions is strongly affected by the type and efficiency of the EET mechanism that is utilized. In some instances, microbes will not

Acknowledgements

Financial support for this work was provided through a CAREER award of the National Science Foundation to L.T.A. (Grant No. 0939882). M.V.’s visit at Cornell University was partially supported by the PhD School in “Industrial Chemical Processes” of Sapienza University of Rome. M.V. acknowledges her PhD advisor Prof. Mauro Majone for the fruitful discussions on biocathode applications and for the comments on the manuscript.

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    These authors contributed equally to this work.

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